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Abstract The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoebaDictyostelium discoideum, certain strains ofBurkholderiabacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. SomeBurkholderiastrains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence ofBurkholderiasymbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates ofD. discoideumand found 25% infected withBurkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions byBurkholderiato the symbiotic lifestyle. Finally, we tested the ability of 38 strains ofBurkholderiafromD. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis inD. discoideum. OnlyD. discoideumnative isolates belonging to theBurkholderia agricolaris,B. hayleyella, andB. bonnieaspecies were able to form persistent symbiotic associations withD. discoideum.TheBurkholderia–Dictyosteliumrelationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.
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Repeated horizontal acquisition of lagriamide-producing symbionts in Lagriinae beetles
Abstract Microbial symbionts associate with multicellular organisms on a continuum from facultative associations to mutual codependency. In the oldest intracellular symbioses there is exclusive vertical symbiont transmission, and co-diversification of symbiotic partners over millions of years. Such symbionts often undergo genome reduction due to low effective population sizes, frequent population bottlenecks, and reduced purifying selection. Here, we describe multiple independent acquisition events of closely related defensive symbionts followed by genome erosion in a group of Lagriinae beetles. Previous work in Lagria villosa revealed the dominant genome-eroded symbiont of the genus Burkholderia produces the antifungal compound lagriamide, protecting the beetle’s eggs and larvae from antagonistic fungi. Here, we use metagenomics to assemble 11 additional genomes of lagriamide-producing symbionts from 7 different host species within Lagriinae from 5 countries, to unravel the evolutionary history of this symbiotic relationship. In each host, we detected one dominant genome-eroded Burkholderia symbiont encoding the lagriamide biosynthetic gene cluster. However, we did not find evidence for host–symbiont co-diversification or for monophyly of the lagriamide-producing symbionts. Instead, our analyses support a single ancestral acquisition of the gene cluster followed by at least four independent symbiont acquisitions and subsequent genome erosion in each lineage. By contrast, a clade of plant-associated relatives retained large genomes but secondarily lost the lagriamide gene cluster. Our results, therefore, reveal a dynamic evolutionary history with multiple independent symbiont acquisitions characterized by a high degree of specificity and highlight the importance of the specialized metabolite lagriamide for the establishment and maintenance of this defensive symbiosis.
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- Award ID(s):
- 1845890
- PAR ID:
- 10554050
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 18
- Issue:
- 1
- ISSN:
- 1751-7362
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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